Sensorimotor cortex excitability and connectivity in Alzheimer's disease: A TMS-EEG Co-registration study

Human Brain Mapping

Volumn 37, Issue 6, 2016, Pages 2083-2096

  Ferreri, Florinda ^a,b   Vecchio, Fabrizio ^c   Vollero, Luca ^a   Guerra, Andrea ^a   Petrichella, Sara ^a   Ponzo, David ^a,b   Määtta, Sara ^b   Mervaala, Esa ^b   Könönen, Mervi ^b   Ursini, Francesca ^a   Pasqualetti, Patrizio ^c,d   Iannello, Giulio ^a   Rossini, Paolo Maria ^c,e   Di Lazzaro, Vincenzo ^a  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

^c IRCCS SAN RAFFAELE PISANA   (Italy)

^d IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^e CATHOLIC UNIVERSITY   (Italy)

Author keywords

Alzheimer's disease; EEG; Navigated transcranial magnetic stimulation; Sensorimotor cortex connectivity; Sensorimotor cortex excitability

Indexed keywords

ACTION POTENTIAL AMPLITUDE; AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONNECTOME; ELECTROENCEPHALOGRAPH; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; FEMALE; HUMAN; LOW RESOLUTION BRAIN ELECTROMAGNETIC TOMOGRAPHY; MALE; MOTOR EVOKED POTENTIAL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; STIMULUS RESPONSE; TRANSCRANIAL MAGNETIC STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION SYSTEM; NERVE TRACT; PATHOPHYSIOLOGY; PROCEDURES; SIGNAL PROCESSING;

AGED; ALZHEIMER DISEASE; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; NEURAL PATHWAYS; SENSORIMOTOR CORTEX; SIGNAL PROCESSING, COMPUTER-ASSISTED; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84959466364     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23158     Document Type: Article

References (69)

1. Abuhassan K, Coyle D, Maguire L (2014): Compensating for thalamocortical synaptic loss in Alzheimer's disease. Front Comput Neurosci 8:65
2. Arendt T (2009): Synaptic degeneration in Alzheimer's disease. Acta Neuropathol 118:167-179.
3. Basso D, Lotze M, Vitale L, Ferreri F, Bisiacchi P, Olivetti Belardinelli M, Rossini PM, Birbaumer N (2006): The role of prefrontal cortex in visuo-spatial planning: A repetitive TMS study. Exp Brain Res 171:411-415.
4. Bella R, Ferri R, Pennisi M, Cantone M, Lanza G, Malaguarnera G, Spampinato C, Giordano D, Alagona G, Pennisi G. (2011): Enhanced motor cortex facilitation in patients with vascular cognitive impairment-no dementia. Neurosci Lett 503:171-175.
5. Bender S, Basseler K, Sebastian I, Resch F, Kammer T, Oelkers-Ax R, Weisbrod M. (2005): Electroencephalographic response to transcranial magnetic stimulation in children: Evidence for giant inhibitory potentials. Ann Neurol 58:58-67.
6. Bozzali M, Parker GJ, Spanò B, Serra L, Giulietti G, Perri R, Magnani G, Marra C, G Vita M, Caltagirone C, Cercignani M. (2013): Brain tissue modifications induced by cholinergic therapy in Alzheimer's disease. Hum Brain Mapp 34:3158-3167.
7. Bonnì S, Lupo F, Lo Gerfo E, Martorana A, Perri R, Caltagirone C, Koch G. (2013): Altered parietal-motor connections in Alzheimer's disease patients. J Alzheimers Dis 33:525-533.
8. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O. (2008): Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321:1686-1689.
9. Cantone M, Di Pino G, Capone F, Piombo M, Chiarello D, Cheeran B, Pennisi G, Di Lazzaro V. (2014): The contribution of transcranial magnetic stimulation in the diagnosis and in the management of dementia. Clin Neurophysiol 125:1509-1532.
10. Carretié L, Tapia M, Mercado F, Albert J, López-Martin S, de la Serna JM. (2004): Voltage-based versus factor score-based source localization analyses of electrophysiological brain activity: A comparison. Brain Topogr 17:109-115.
11. D'Amelio M, Rossini PM (2012): Brain excitability and connectivity of neuronal assemblies in Alzheimer's disease: From animal models to human findings. Prog Neurobiol 99:42-60. Review.
12. Delbeuck X, Van der Linden M, Collette F (2003): Alzheimer's disease as a disconnection syndrome? Neuropsychol Rev 13:79-92.
13. Delorme A, Makeig S (2004): EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9-21.
14. Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, Saturno E, Pilato F, Masullo C, Rothwell JC. (2002): Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology 59:392-397.
15. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Daniele A, Ghirlanda S, Gainotti G, Tonali PA. (2004): Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer's disease. J Neurol Neurosurg Psychiatry 75:555-559.
16. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Ghirlanda S, Ranieri F, Gainotti G, Tonali P. (2005): Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 76:1064-1069.
17. Di Pino G, Pellegrino G, Assenza G, Capone F, Ferreri F, Formica D, Ranieri F, Tombini M, Ziemann U, Rothwell JC, Di Lazzaro V. (2014): Modulation of brain plasticity in stroke: A novel model for neurorehabilitation. Nat Rev Neurol 10:597-608.
18. Elman JA, Oh H, Madison CM, Baker SL, Vogel JW, Marks SM, Crowley S, O'Neil JP, Jagust WJ. (2014): Neural compensation in older people with brain amyloid-βdeposition. Nat Neurosci 17:1316-1318.
19. Feig S, Lipton P (1993): Pairing the cholinergic agonist carbachol with patterned Schaffer collateral stimulation initiates protein synthesis in hippocampal CA1 pyramidal cell dendrites via a muscarinic, NMDA-dependent mechanism. J Neurosci 13:1010-1021.
20. Ferreri F, Pauri F, Pasqualetti P, Fini R, Dal Forno G, Rossini PM. (2003): Motor cortex excitability in Alzheimer's disease: A transcranial magnetic stimulation study. Ann Neurol 53:102-108.
21. Ferreri F, Curcio G, Pasqualetti P, De Gennaro L, Fini R, Rossini PM. (2006): Mobile phone emissions and human brain excitability. Ann Neurol 60:188-196.
22. Ferreri F, Pasqualetti P, Määttä S, Ponzo D, Guerra A, Bressi F, Chiovenda P, Del Duca M, Giambattistelli F, Ursini F, Tombini M, Vernieri F, Rossini PM. (2011a): Motor cortex excitability in Alzheimer's disease: A transcranial magnetic stimulation follow-up study. Neurosci Lett 492:94-98.
23. Ferreri F, Pasqualetti P, Määttä S, Ponzo D, Ferrarelli F, Tononi G, Mervaala E, Miniussi C, Rossini PM. (2011b): Human brain connectivity during single and paired pulse transcranial magnetic stimulation. Neuroimage 54:90-102.
24. Ferreri F, Ponzo D, Hukkanen T, Mervaala E, Könönen M, Pasqualetti P, Vecchio F, Rossini PM, Määttä S. (2012): Human brain cortical correlates of short-latency afferent inhibition: A combined EEG-TMS study. J Neurophysiol 108:314-323.
25. Ferreri F, Rossini PM (2013): TMS and TMS-EEG techniques in the study of the excitability, connectivity, and plasticity of the human motor cortex. Rev Neurosci 24:431-442.
26. Ferreri F, Vecchio F, Ponzo D, Pasqualetti P, Rossini PM (2014a): Time-varying coupling of EEG oscillations predicts excitability fluctuations in the primary motor cortex as reflected by motor evoked potentials amplitude: An EEG-TMS study. Hum Brain Mapp 35:1969-1980.
27. Ferreri F, Ponzo D, Vollero L, Guerra A, Di Pino G, Petrichella S, Benvenuto A, Tombini M, Rossini L, Denaro L, Micera S, Iannello G, Guglielmelli E, Denaro V, Rossini PM. (2014b): Does an intraneural interface short-term implant for robotic hand control modulate sensorimotor cortical integration? An EEG-TMS co-registration study on a human amputee. Restor Neurol Neurosci 32:281-292.
28. Fjell AM, Walhovd KB (2010): Structural brain changes in aging: Courses, causes and cognitive consequences. Rev Neurosci 21:187-221.
29. Golaz J, Bouras C, Hof PR (1992): Motor cortex involvement in presenile dementia: Report of a case. J Geriatr Psychiatry Neurol 5:85-92.
30. Grutzendler J, Helmin K, Tsai J, Gan WB (2007): Various dendritic abnormalities are associated with fibrillar amyloid deposits in Alzheimer's disease. Ann N Y Acad Sci 1097:30-39.
31. Guerra A, Assenza F, Bressi F, Scrascia F, Del Duca M, Ursini F, Vollaro S, Trotta L, Tombini M, Chisari C, Ferreri F. (2011): Transcranial magnetic stimulation studies in Alzheimer's disease. Int J AlzheimersDis 2011:263817
32. Guerra A, Petrichella S, Vollero L, Ponzo D, Pasqualetti P, Määttä S, Mervaala E, Könönen M, Bressi F, Iannello G, Rossini PM, Ferreri F. (2015): Neurophysiological features of motor cortex excitability and plasticity in subcortical ischemic vascular dementia: A TMS mapping study. Clin Neurophysiol pii: S1388-2457(14)00477-5.
33. He Y, Chen Z, Gong G, Evans A (2009): Neuronal networks in Alzheimer's disease. Neuroscientist 15:333-350.
34. Hoeppner J, Wegrzyn M, Thome J, Bauer A, Oltmann I, Buchmann J, Teipel S. (2012): Intra- and inter-cortical motor excitability in Alzheimer's disease. J Neural Transm 119:605-612.
35. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Näätänen R, Katila T. (1997): Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8:3537-3540.
36. Julkunen P, Jauhiainen AM, Westerén-Punnonen S, Pirinen E, Soininen H, Könönen M, Pääkkönen A, Määttä S, Karhu J. (2008): Navigated TMS combined with EEG in mild cognitive impairment and Alzheimer's disease: A pilot study. J Neurosci Methods 172:270-276.
37. Julkunen P, Jauhiainen AM, Könönen M, Pääkkönen A, Karhu J, Soininen H (2011): Combining transcranial magnetic stimulation and electroencephalography may contribute to assess the severity of Alzheimer's disease. Int J Alzheimers Dis 654794
38. Kellner V, Menkes-Caspi N, Beker S, Stern EA (2014): Amyloid-β alters ongoing neuronal activity and excitability in the frontal cortex. Neurobiol Aging 35:1982-1991. Sep;
39. Khedr EM, Ahmed MA, Darwish ES, Ali AM (2011): The relationship between motor cortex excitability and severity of Alzheimer's disease: A transcranial magnetic stimulation study. Neurophysiol Clin 41:107-113.
40. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, Micheva KD, Smith SJ, Kim ML, Lee VM, Hyman BT, Spires-Jones TL. (2009): Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. ProcNatlAcadSci U S A 10;106:4012-4017.
41. Komssi S, Kähkönen S, Ilmoniemi RJ (2004): The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp 21:154-164.
42. Komssi S, Kähkönen S (2006): The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev 52:183-192.
43. Lehmann D, Skrandies W (1980): Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48:609-621.
44. Liepert J, Bär KJ, Meske U, Weiller C. (2001): Motor cortex disinhibition in Alzheimer's disease. Clin Neurophysiol 112:1436-1441.
45. Litvak V, Komssi S, Scherg M, Hoechstetter K, Classen J, Zaaroor M, Pratt H, Kahkonen S. (2007): Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex. Neuroimage 37:56-70.
46. Mäki H, Ilmoniemi RJ (2010): The relationship between peripheral and early cortical activation induced by transcranial magnetic stimulation. NeurosciLett 478:24-28.
47. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. (2005): Breakdown of cortical effective connectivity during sleep. Science 30;309:2228-2232.
48. Mastrangelo MA, Bowers WJ (2008): Detailed immuno-histochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice. BMC Neurosci 9:81
49. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH. (2011): The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7:263-269. May;
50. Oh H, Jagust WJ (2013): Frontotemporal network connectivity during memory encoding is increased with aging and disrupted by beta-amyloid. J Neurosci 20;33:18425-18437.
51. Palop JJ, Mucke L (2010): Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: From synapses toward neural networks. Nat Neurosci 13:812-818.
52. Pascual-Marqui RD, Esslen M, Kochi K, Lehmann D (2002): Functional imaging with low-resolution brain electromagnetic tomography (LORETA): A review. Methods Find ExpClin Pharmacol 24 Suppl C:91-95.
53. Paula-Lima AC, Brito-Moreira J, Ferreira ST (2013): Deregulation of excitatory neurotransmission underlying synapse failure in Alzheimer's disease. J Neurochem 126:191-202.
54. Paus T, Sipilä PK, Strafella AP (2001): Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: An EEG study. J Neurophysiol 86:1983-1990.
55. Polania R, Paulus W, Antal A, Nitsche MA (2011): Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study. Neuroimage 54:2287-2296.
56. Rossini PM, Ferilli MA, Rossini L, Ferreri F (2013): Clinical neurophysiology of brain plasticity in aging brain. Curr Pharm Des 19:6426-6439. Review.
57. Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, Di Lazzaro V, Ferreri F, Fitzgerald PB, George MS, Hallett M, Lefaucheur JP, Langguth B, Matsumoto H, Miniussi C, Nitsche MA, Pascual-Leone A, Paulus W, Rossi S, Rothwell JC, Siebner HR, Ugawa Y, Walsh V, Ziemann U. (2015): Twenty years after: Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: Basic principles and procedures for routine clinical application. An updated report from an I.F.C.N. committee. Clin Neurophysiol 126:1071-1107.
58. Salmaso D, Longoni AM (1985): Problems in the assessment of hand preference. Cortex 21:533-549.
59. Sanes JN, Donoghue JP (2000): Plasticity and primary motor cortex. Annu Rev Neurosci 23:393-415.
60. Suvà D, Favre I, Kraftsik R, Esteban M, Lobrinus A, Miklossy J. (1999): Primary motor cortex involvement in Alzheimer disease. J Neuropathol Exp Neurol 58:1125-1134.
61. Teitti S, Määttä S, Säisänen L, Könönen M, Vanninen R, Hannula H, Mervaala E, Karhu J (2008): Non-primary motor areas in the human frontal lobe are connected directly to hand muscles. Neuroimage 40:1243
62. Vaalto S, Säisänen L, Könönen M, Julkunen P, Hukkanen T, Määttä S, Karhu J (2011): Corticospinal output and cortical excitation-inhibition balance in distal hand muscle representations in nonprimary motor area. Hum Brain Mapp 32:1692-1703.
63. Van Der Werf YD, Paus T (2006): The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp Brain Res 175:231-245.
64. Van Der Werf YD, Sadikot AF, Strafella AP, Paus T (2006): The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions. Exp Brain Res 175:246-255.
65. Vecchio F, Määttä S (2011): The use of auditory event-related potentials in Alzheimer's disease diagnosis. Int J Alzheimers Dis 2011:653173
66. Vecchio F, Babiloni C, Lizio R, Fallani Fde V, Blinowska K, Verrienti G, Frisoni G, Rossini PM. (2013): Resting state cortical EEG rhythms in Alzheimer's disease: Toward EEG markers for clinical applications: A review. Suppl Clin Neurophysiol 62:223-236.
67. Veniero D, Bortoletto M, Miniussi C (2009): TMS-EEG co-registration: On TMS-induced artefact. ClinNeurophysiol 1392-1399.
68. Xiang Z, Huguenard JR, Prince DA (1998): Cholinergic switching within neocortical inhibitory networks. Science 281:985-988.
69. Yuan Q, Su H, Zhang Y, Chau WH, Ng CT, Song YQ, Huang JD, Wu W, Lin ZX. (2013): Amyloid pathology in spinal cord of the transgenic Alzheimer's disease mice is correlated to the corticospinal tract pathway. J Alzheimers Dis 35:675-685.